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Angiosperm Phylogeny: 17 Genes, 640 Taxa

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Angiosperm Phylogeny: 17 Genes, 640 Taxa American Journal of Botany 98(4): 704–730. 2011. A NGIOSPERM PHYLOGENY: 17 GENES, 640 TAXA 1 Douglas E. Soltis 2,19 , Stephen A. Smith 3 , Nico Cellinese 4 , Kenneth J. Wurdack 5 , David C. Tank 6 , Samuel F. Brockington 7 , Nancy F. Refulio-Rodriguez 8 , Jay B. Walker 9 , Michael J. Moore 10 , Barbara S. Carlsward 11 , Charles D. Bell 12 , Maribeth Latvis 2,4 , Sunny Crawley 13 , Chelsea Black 13 , Diaga Diouf 13,14 , Zhenxiang Xi 15 , Catherine A. Rushworth 15 , Matthew A. Gitzendanner2,4 , Kenneth J. Sytsma 9 , Yin-Long Qiu 16 , Khidir W. Hilu13 , Charles C. Davis 15 , Michael J. Sanderson 17 , Reed S. Beaman 4 , Richard G. Olmstead 8 , Walter S. Judd2 , Michael J. Donoghue 18 , and Pamela S. Soltis 4 2 Department of Biology, University of Florida, Gainesville, Florida 32611-8525 USA; 3 Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912 USA; 4 Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 USA; 5 Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013-7012 USA; 6 Department of Forest Ecology and Biogeosciences & Stillinger Herbarium, University of Idaho, P. O. Box 441133, Moscow, Idaho 83844-1133 USA; 7 Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK; 8 Department of Biology, University of Washington, Seattle, Washington 98195-5325 USA; 9 Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA; 10 Biology Department, Oberlin College, Oberlin, Ohio 44074-1097 USA; 11 Department of Biological Sciences, Eastern Illinois University, Charleston, Illinois 61920 USA; 12 Department of Biological Sciences, University of New Orleans, New Orleans, Louisiana 70148 USA; 13 Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 USA; 14 D é partement de Biologie V é g é tale, Universit é Cheikh AntDeara Diop, Dakar – Fann, BP 5005, Republic of S é n é gal; 15 Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts 02138 USA; 16 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109-1048 USA; 17 Department of Ecology and Evolutionary Biology, University of Arizona, 1041 East Lowell, Tucson, Arizona 85721-0088 USA; and 18 Department of Ecology and Evolutionary Biology, Yale University, P. O. Box 208106, New Haven, Connecticut 06520-8106 USA • Premise of the study : Recent analyses employing up to fi ve genes have provided numerous insights into angiosperm phylogeny, but many relationships have remained unresolved or poorly supported. In the hope of improving our understanding of angio- sperm phylogeny, we expanded sampling of taxa and genes beyond previous analyses. • Methods : We conducted two primary analyses based on 640 species representing 330 families. The fi rst included 25 260 aligned base pairs (bp) from 17 genes (representing all three plant genomes, i.e., nucleus, plastid, and mitochondrion). The second included 19 846 aligned bp from 13 genes (representing only the nucleus and plastid). • Key results : Many important questions of deep-level relationships in the nonmonocot angiosperms have now been resolved with strong support. Amborellaceae, Nymphaeales, and Austrobaileyales are successive sisters to the remaining angiosperms ( Mesangiospermae ), which are resolved into Chloranthales + Magnoliidae as sister to Monocotyledoneae + [Ceratophyllaceae + Eudicotyledoneae ]. Eudicotyledoneae contains a basal grade subtending Gunneridae . Within Gunneridae , Gunnerales are sis- ter to the remainder ( Pentapetalae ), which comprises (1) Superrosidae , consisting of Rosidae (including Vitaceae) and Saxi- fragales; and (2) Superasteridae , comprising Berberidopsidales, Santalales, Caryophyllales , Asteridae , and, based on this study, Dilleniaceae (although other recent analyses disagree with this placement). Within the major subclades of Pentapetalae , most deep-level relationships are resolved with strong support. • Conclusions : Our analyses confi rm that with large amounts of sequence data, most deep-level relationships within the angio- sperms can be resolved. We anticipate that this well-resolved angiosperm tree will be of broad utility for many areas of biology, including physiology, ecology, paleobiology, and genomics. Key words: angiosperms; bioinformatics; large data sets; molecular systematics; RAxML; S uperasteridae ; supermatrix; Superrosidae . 1 Manuscript received 11 October 2010; revision accepted 9 February 2011. C.C.D., DEB-9634231; EF-0431057 to K.H., EF-0431233 to K.J.S., The authors thank the University of Florida High-Performance DEB-0431239 to Y.L.Q.) with additional support from NSF grant DEB- Computing Center, the UF Genetics Institute, and facilities supported in 0544039 to C.C.D. The authors thank the Royal Botanic Gardens, Kew, part by NSF Grant CNS-0821622 for providing computational resources and the Missouri Botanical Garden for providing samples used in this that facilitated the completion of this research. The authors thank E. study. Mavrodiev for help in preparing some of the fi gures. This study was 19 Author for correspondence (e-mail: [email protected]fl .edu) carried out as part of the Angiosperm Tree of Life Project (NSF EF- 0431266 to D.E.S., P.S.S., W.S.J., and S. R. Manchester, EF-0431242 to doi:10.3732/ajb.1000404 American Journal of Botany 98(4): 704–730, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 704 April 2011] Soltis et al. — Angiosperm phylogeny 705 It has been a decade since the 567-taxon, three-gene (rbcL, MATERIALS AND METHODS atpB , and 18S rDNA) parsimony-based phylogenetic analysis of angiosperms was published ( Soltis et al., 1999 , 2000 ). Since Data sets— DNA samples for most of the species used here were extracted that time, other studies have expanded sampling of additional from either fresh or silica-dried material following the general method of Doyle genes or used alternative methods to evaluate the results of that and Doyle (1987) or modifi cations thereof that employ liquid nitrogen and higher CTAB concentrations (e.g., Soltis et al., 1991 ; Sytsma, 1994 ). We at- three-gene study. Hilu et al. (2003) conducted a broad analysis tempted to use the same species and DNA samples across all of the genes ana- of angiosperms based on matK sequences, with results that lyzed here, although multiple species were sometimes used as necessary agreed closely with the three-gene topology. Additional prog- placeholders to reduce missing data. Many of these DNA samples have been ress was achieved by Davies et al. (2004) by constructing a used in earlier analyses (e.g., Chase et al., 1993 ; Soltis et al., 2000 ). supertree for angiosperms. Soltis et al. (2007) undertook a We constructed a 17-gene data set for 640 species (for a complete list of taxa, Bayesian analysis of the 567-taxon, three-gene data set and ob- voucher information, and GenBank numbers see Appendix S1, see Supple- mental Data online at http://www.amjbot.org/cgi/content/full/ajb.1000404/DC1) tained a topology nearly identical to that obtained with parsi- using genes from the nuclear, plastid, and mitochondrial genomes. Given mony. More recently, Bell et al. (2010) analyzed this same the potential problems inherent in phylogeny reconstruction using mtDNA se- three-gene data set using a Bayesian relaxed clock model to si- quences (e.g., RNA editing, Bowe and dePamphilis, 1996 ; horizontal gene multaneously infer topology and divergence times within an- transfer or HGT, Bergthorsson et al., 2003 ), we also constructed a data set giosperms and found results similar to Soltis et al. (2007) . In without the mtDNA data, resulting in a matrix of 13 genes. For both data sets, addition, Burleigh et al. (2009) inferred angiosperm phylogeny we used the following representatives of Acrogymnospermae (extant gymno- sperms, sensu Cantino et al., 2007 ) as the outgroup: Cycas , Ginkgo , Gnetum , using fi ve genes for the same 567 taxa analyzed in Soltis et al. Metasequoia , Pinus , Podocarpus , Welwitschia , and Zamia. Taxon sampling (1999 , 2000 ). Although the fi ve-gene matrix had signifi cantly across major clades of angiosperms was not uniform, with poorly resolved more missing data (27.5%) than the three-gene matrix (2.9%), clades (e.g., Malpighiales, Saxifragales) targeted for denser taxon sampling to the fi ve-gene analysis resulted in higher levels of bootstrap sup- seek improved resolution. We also largely avoided parasitic clades (except port across the tree. Orobanchaceae, Santalales, and Cuscuta ), which can create analytical prob- lems due to gene loss, accelerated molecular evolution, and horizontal gene Recent phylogenomic analyses have shown the value of con- transfer (see Davis and Wurdack, 2004 ; Nickrent et al., 2004 ; Barkman et al., structing data sets of many genes to infer deep-level angiosperm 2007 ). phylogeny. Some of these analyses have employed nearly com- The following 17 genes were sequenced: 18S and 26S rDNA from the plete plastid genome sequence data (e.g., Leebens-Mack et al., nuclear genome; atpB , matK , ndhF , psbBTNH (four contiguous genes here treated 2005 ; Jansen et al., 2007 ; Moore et al., 2007 , 2010 ), but all as one region), rbcL , rpoC2 , rps16 , and rps4 from the plastid genome; and atp1 , have been limited in sampling to fewer than 100 taxa. These matR , nad5 , and rps3 from the mitochondrial genome. The total length of the aligned 17-gene matrix was 25 260 bp and of the 13-gene matrix was 19 846 bp. and other studies based on many genes but focused only on The percentage of missing data for the full data set was 41% and for the data set major angiosperm clades (e.g., Sch ö nenberger et al., 2005 ; Jian without mtDNA data was 42%. et al., 2008 ; H. Wang et al., 2009 ; Wurdack and Davis, 2009 ; Brockington et al., 2010 ; Tank and Donoghue, 2010 ) showed Alignment and phylogenetic analyses— All sequence data were stored and that with very large amounts of data (i.e., 13 to 83 genes), many, managed in TOLKIN ( Beaman and Cellinese, 2010 ).
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